Assembly of Large Icosahedral Double-Stranded RNA Viruses

  • Chapter
  • First Online:
Viral Molecular Machines

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 726))

Abstract

Double-stranded RNA (dsRNA) viruses are a diverse group of viruses infecting hosts from bacteria to higher eukaryotes. Among the hosts are humans, domestic animals, and economically important plant species. Fine details of high-resolution virion structures have revealed common structural characteristics unique to these viruses including an internal icosahedral capsid built from 60 asymmetric dimers (120 monomers!) of the major coat protein. Here we focus mainly on the structures and assembly principles of large icosahedral dsRNA viruses belonging to the families of Cystoviridae and Reoviridae. It is obvious that there are a variety of assembly pathways utilized by different viruses starting from similar building blocks and reaching in all cases a similar capsid architecture. This is true even with closely related viruses indicating that the assembly pathway per se is not an indicator of relatedness and is achieved with minor changes in the interacting components.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
GBP 19.95
Price includes VAT (United Kingdom)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
GBP 143.50
Price includes VAT (United Kingdom)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
GBP 179.99
Price includes VAT (United Kingdom)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
GBP 179.99
Price includes VAT (United Kingdom)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

dsRNA:

Double-stranded RNA

mRNA:

Messenger RNA

ssRNA:

Single-stranded RNA

Cryo-EM:

Cryo-electron microscopy

References

  • Altenburg BC, Graham DY, Estes MK (1980) Ultrastructural study of rotavirus replication in cultured cells. J Gen Virol 46:75–85

    Article  PubMed  CAS  Google Scholar 

  • Bamford DH (2003) Do viruses form lineages across different domains of life? Res Microbiol 154:231–236

    Article  PubMed  CAS  Google Scholar 

  • Bamford DH, Mindich L (1980) Electron microscopy of cells infected with nonsense mutants of bacteriophage Ï•6. Virology 107:222–228

    Article  PubMed  CAS  Google Scholar 

  • Bamford DH, Romantschuk M, Somerharju PJ (1987) Membrane fusion in prokaryotes: bacteriophage Ï•6 membrane fuses with the Pseudomonas syringae outer membrane. EMBO J 6:1467–1473

    PubMed  CAS  Google Scholar 

  • Bamford JK, Bamford DH, Li T, Thomas GJ Jr (1993) Structural studies of the enveloped dsRNA bacteriophage Ï•6 of Pseudomonas syringae by Raman spectroscopy. II. Nucleocapsid structure and thermostability of the virion, nucleocapsid and polymerase complex. J Mol Biol 230:473–482

    Article  PubMed  CAS  Google Scholar 

  • Banerjee AK, Shatkin AJ (1970) Transcription in vitro by reovirus-associated ribonucleic acid-dependent polymerase. J Virol 6:1–11

    Article  PubMed  CAS  Google Scholar 

  • Basak AK, Stuart DI, Roy P (1992) Preliminary crystallographic study of bluetongue virus capsid protein, VP7. J Mol Biol 228:687–689

    Article  PubMed  CAS  Google Scholar 

  • Becker MM, Peters TR, Dermody TS (2003) Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J Virol 77:5948–5963

    Article  PubMed  CAS  Google Scholar 

  • Benevides JM, Juuti JT, Tuma R, Bamford DH, Thomas GJ Jr (2002) Characterization of subunit-specific interactions in a double-stranded RNA virus: Raman difference spectroscopy of the Ï•6 procapsid. Biochemistry 41:11946–11953

    Article  PubMed  CAS  Google Scholar 

  • Berois M, Sapin C, Erk I, Poncet D, Cohen J (2003) Rotavirus nonstructural protein NSP5 interacts with major core protein VP2. J Virol 77:1757–1763

    Article  PubMed  CAS  Google Scholar 

  • Bican P, Cohen J, Charpilienne A, Scherrer R (1982) Purification and characterization of bovine rotavirus cores. J Virol 43:1113–1117

    PubMed  CAS  Google Scholar 

  • Bisaillon M, Bergeron J, Lemay G (1997) Characterization of the nucleoside triphosphate phosphohydrolase and helicase activities of the reovirus λ1 protein. J Biol Chem 272:18298–18303

    Article  PubMed  CAS  Google Scholar 

  • Bottcher B, Kiselev NA, Stel’Mashchuk VY, Perevozchikova NA, Borisov AV, Crowther RA (1997) Three-dimensional structure of infectious bursal disease virus determined by electron cryomicroscopy. J Virol 71:325–330

    PubMed  CAS  Google Scholar 

  • Brookes SM, Hyatt AD, Eaton BT (1993) Characterization of virus inclusion bodies in bluetongue virus-infected cells. J Gen Virol 74:525–530

    Article  PubMed  Google Scholar 

  • Burroughs JN, O’Hara RS, Smale CJ, Hamblin C, Walton A, Armstrong R, Mertens PP (1994) Purification and properties of virus particles, infectious subviral particles, cores and VP7 crystals of African horsesickness virus serotype 9. J Gen Virol 75:1849–1857

    Article  PubMed  CAS  Google Scholar 

  • Butan C, Tucker P (2010) Insights into the role of the non-structural protein 2 (NS2) in Bluetongue virus morphogenesis. Virus Res 151:109–117

    Article  PubMed  CAS  Google Scholar 

  • Butcher SJ, Dokland T, Ojala PM, Bamford DH, Fuller SD (1997) Intermediates in the assembly pathway of the double-stranded RNA virus Ï•6. EMBO J 16:4477–4487

    Article  PubMed  CAS  Google Scholar 

  • Butcher SJ, Grimes JM, Makeyev EV, Bamford DH, Stuart DI (2001) A mechanism for initiating RNA-dependent RNA polymerization. Nature 410:235–240

    Article  PubMed  CAS  Google Scholar 

  • Calvert JG, Nagy E, Soler M, Dobos P (1991) Characterization of the VPg-dsRNA linkage of infectious pancreatic necrosis virus. J Gen Virol 72:2563–2567

    Article  PubMed  CAS  Google Scholar 

  • Carstens EB (2010) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch Virol 155:133–146

    Article  PubMed  CAS  Google Scholar 

  • Caston JR, Ghabrial SA, Jiang D, Rivas G, Alfonso C, Roca R, Luque D, Carrascosa JL (2003) Three-dimensional structure of Penicillium chrysogenum virus: a double-stranded RNA virus with a genuine T  =  1 capsid. J Mol Biol 331:417–431

    Article  PubMed  CAS  Google Scholar 

  • Chandra R (1997) Picobirnavirus, a novel group of undescribed viruses of mammals and birds: a minireview. Acta Virol 41:59–62

    PubMed  CAS  Google Scholar 

  • Chandran K, Walker SB, Chen Y, Contreras CM, Schiff LA, Baker TS, Nibert ML (1999) In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3. J Virol 73:3941–3950

    PubMed  CAS  Google Scholar 

  • Chappell JD, Prota AE, Dermody TS, Stehle T (2002) Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J 21:1–11

    Article  PubMed  CAS  Google Scholar 

  • Charpilienne A, Lepault J, Rey F, Cohen J (2002) Identification of rotavirus VP6 residues located at the interface with VP2 that are essential for capsid assembly and transcriptase activity. J Virol 76:7822–7831

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Luongo CL, Nibert ML, Patton JT (1999) Rotavirus open cores catalyze 5′-cap** and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 265:120–130

    Article  PubMed  CAS  Google Scholar 

  • Cheng RH, Caston JR, Wang GJ, Gu F, Smith TJ, Baker TS, Bozarth RF, Trus BL, Cheng N, Wickner RB et al (1994) Fungal virus capsids, cytoplasmic compartments for the replication of double-stranded RNA, formed as icosahedral shells of asymmetric Gag dimers. J Mol Biol 244:255–258

    Article  PubMed  CAS  Google Scholar 

  • Cheng L, Zhu J, Hui WH, Zhang X, Honig B, Fang Q, Zhou ZH (2010) Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. J Mol Biol 397:852–863

    Article  PubMed  CAS  Google Scholar 

  • Cleveland DR, Zarbl H, Millward S (1986) Reovirus guanylyltransferase is L2 gene product lambda 2. J Virol 60:307–311

    PubMed  CAS  Google Scholar 

  • Coombs KM (1996) Identification and characterization of a double-stranded RNA− reovirus temperature-sensitive mutant defective in minor core protein μ2. J Virol 70:4237–4245

    PubMed  CAS  Google Scholar 

  • Coulibaly F, Chevalier C, Gutsche I, Pous J, Navaza J, Bressanelli S, Delmas B, Rey FA (2005) The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell 120:761–772

    Article  PubMed  CAS  Google Scholar 

  • Coulibaly F, Chiu E, Ikeda K, Gutmann S, Haebel PW, Schulze-Briese C, Mori H, Metcalf P (2007) The molecular organization of cypovirus polyhedra. Nature 446:97–101

    Article  PubMed  CAS  Google Scholar 

  • Coulibaly F, Chevalier C, Delmas B, Rey FA (2010) Crystal structure of an Aquabirnavirus particle: insights into antigenic diversity and virulence determinism. J Virol 84:1792–1799

    Article  PubMed  CAS  Google Scholar 

  • Cvirkaite-Krupovic V, Poranen MM, Bamford DH (2010) Phospholipids act as secondary receptor during the entry of the enveloped, double-stranded RNA bacteriophage phi6. J Gen Virol 91:2116–2120

    Article  PubMed  CAS  Google Scholar 

  • de Haas F, Paatero AO, Mindich L, Bamford DH, Fuller SD (1999) A symmetry mismatch at the site of RNA packaging in the polymerase complex of dsRNA bacteriophage Ï•6. J Mol Biol 294:357–372

    Article  PubMed  CAS  Google Scholar 

  • Dinman JD, Icho T, Wickner RB (1991) A 1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc Natl Acad Sci USA 88:174–178

    Article  PubMed  CAS  Google Scholar 

  • Diprose JM, Burroughs JN, Sutton GC, Goldsmith A, Gouet P, Malby R, Overton I, Zientara S, Mertens PP, Stuart DI, Grimes JM (2001) Translocation portals for the substrates and products of a viral transcription complex: the bluetongue virus core. EMBO J 20:7229–7239

    Article  PubMed  CAS  Google Scholar 

  • Dryden KA, Wang G, Yeager M, Nibert ML, Coombs KM, Furlong DB, Fields BN, Baker TS (1993) Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J Cell Biol 122:1023–1041

    Article  PubMed  CAS  Google Scholar 

  • Dryden KA, Farsetta DL, Wang G, Keegan JM, Fields BN, Baker TS, Nibert ML (1998) Internal/structures containing transcriptase-related proteins in top component particles of mammalian orthoreovirus. Virology 245:33–46

    Article  PubMed  CAS  Google Scholar 

  • Duquerroy S, Da Costa B, Henry C, Vigouroux A, Libersou S, Lepault J, Navaza J, Delmas B, Rey FA (2009) The picobirnavirus crystal structure provides functional insights into virion assembly and cell entry. EMBO J 28:1655–1665

    Article  PubMed  CAS  Google Scholar 

  • Ewen ME, Revel HR (1988) In vitro replication and transcription of the segmented double-stranded RNA bacteriophage Ï•6. Virology 165:489–498

    Article  PubMed  CAS  Google Scholar 

  • Ewen ME, Revel HR (1990) RNA-protein complexes responsible for replication and transcription of the double-stranded RNA bacteriophage Ï•6. Virology 178:509–519

    Article  PubMed  CAS  Google Scholar 

  • Fabbretti E, Afrikanova I, Vascotto F, Burrone OR (1999) Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J Gen Virol 80:333–339

    PubMed  CAS  Google Scholar 

  • Fraser RD, Furlong DB, Trus BL, Nibert ML, Fields BN, Steven AC (1990) Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J Virol 64:2990–3000

    PubMed  CAS  Google Scholar 

  • Fregolente MC, de Castro-Dias E, Martins SS, Spilki FR, Allegretti SM, Gatti MS (2009) Molecular characterization of picobirnaviruses from new hosts. Virus Res 143:134–136

    Article  PubMed  CAS  Google Scholar 

  • French TJ, Roy P (1990) Synthesis of bluetongue virus (BTV) corelike particles by a recombinant baculovirus expressing the two major structural core proteins of BTV. J Virol 64:1530–1536

    PubMed  CAS  Google Scholar 

  • Frilander M, Bamford DH (1995) In vitro packaging of the single-stranded RNA genomic precursors of the segmented double-stranded RNA bacteriophage Ï•6: the three segments modulate each other’s packaging efficiency. J Mol Biol 246:418–428

    Article  PubMed  CAS  Google Scholar 

  • Frilander M, Gottlieb P, Strassman J, Bamford DH, Mindich L (1992) Dependence of minus-strand synthesis on complete genomic packaging in the double-stranded RNA bacteriophage Ï•6. J Virol 66:5013–5017

    PubMed  CAS  Google Scholar 

  • Frilander M, Poranen M, Bamford DH (1995) The large genome segment of dsRNA bacteriophage Ï•6 is the key regulator in the in vitro minus and plus strand synthesis. RNA 1:510–518

    PubMed  CAS  Google Scholar 

  • Gorziglia M, Larrea C, Liprandi F, Esparza J (1985) Biochemical evidence for the oligomeric (possibly trimeric) structure of the major inner capsid polypeptide (45K) of rotaviruses. J Gen Virol 66:1889–1900

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb P, Metzger S, Romantschuk M, Carton J, Strassman J, Bamford DH, Kalkkinen N, Mindich L (1988a) Nucleotide sequence of the middle dsRNA segment of bacteriophage Ï•6: placement of the genes of membrane-associated proteins. Virology 163:183–190

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb P, Strassman J, Bamford DH, Mindich L (1988b) Production of a polyhedral particle in Escherichia coli from a cDNA copy of the large genomic segment of bacteriophage Ï•6. J Virol 62:181–187

    PubMed  CAS  Google Scholar 

  • Gottlieb P, Strassman J, Qiao X, Frilander M, Frucht A, Mindich L (1992) In vitro packaging and replication of individual genomic segments of bacteriophage Ï•6 RNA. J Virol 66:2611–2616

    PubMed  CAS  Google Scholar 

  • Gottlieb P, Qiao X, Strassman J, Frilander M, Mindich L (1994) Identification of the packaging regions within the genomic RNA segments of bacteriophage Ï•6. Virology 200:42–47

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb P, Wei H, Potgieter C, Toporovsky I (2002) Characterization of Ï•12, a bacteriophage related to Ï•6: nucleotide sequence of the small and middle double-stranded RNA. Virology 293:118–124

    Article  PubMed  CAS  Google Scholar 

  • Gouet P, Diprose JM, Grimes JM, Malby R, Burroughs JN, Zientara S, Stuart DI, Mertens PP (1999) The highly ordered double-stranded RNA genome of bluetongue virus revealed by crystallography. Cell 97:481–490

    Article  PubMed  CAS  Google Scholar 

  • Grimes J, Basak AK, Roy P, Stuart D (1995) The crystal structure of bluetongue virus VP7. Nature 373:167–170

    Article  PubMed  CAS  Google Scholar 

  • Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Zientara S, Mertens PP, Stuart DI (1998) The atomic structure of the bluetongue virus core. Nature 395:470–478

    Article  PubMed  CAS  Google Scholar 

  • Guglielmi KM, McDonald SM, Patton JT (2010) Mechanism of intraparticle synthesis of the rotavirus double-stranded RNA genome. J Biol Chem 285:18123–18128

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara K, Higashi T, Namba K, Uehara-Ichiki T, Omura T (2003) Assembly of single-shelled cores and double-shelled virus-like particles after baculovirus expression of major structural proteins P3, P7 and P8 of Rice dwarf virus. J Gen Virol 84:981–984

    Article  PubMed  CAS  Google Scholar 

  • Hantula J, Bamford DH (1988) Chemical crosslinking of bacteriophage Ï•6 nucleocapsid proteins. Virology 165:482–488

    Article  PubMed  CAS  Google Scholar 

  • Hassan SS, Roy P (1999) Expression and functional characterization of bluetongue virus VP2 protein: role in cell entry. J Virol 73:9832–9842

    PubMed  CAS  Google Scholar 

  • Hassan SH, Wirblich C, Forzan M, Roy P (2001) Expression and functional characterization of bluetongue virus VP5 protein: role in cellular permeabilization. J Virol 75:8356–8367

    Article  PubMed  CAS  Google Scholar 

  • Hewat EA, Booth TF, Loudon PT, Roy P (1992) Three-dimensional reconstruction of baculovirus expressed bluetongue virus core-like particles by cryo-electron microscopy. Virology 189:10–20

    Article  PubMed  CAS  Google Scholar 

  • Hill CL, Booth TF, Prasad BV, Grimes JM, Mertens PP, Sutton GC, Stuart DI (1999) The structure of a cypovirus and the functional organization of dsRNA viruses. Nat Struct Biol 6:565–568

    Article  PubMed  CAS  Google Scholar 

  • Hoogstraten D, Qiao X, Sun Y, Hu A, Onodera S, Mindich L (2000) Characterization of Ï•8, a bacteriophage containing three double-stranded RNA genomic segments and distantly related to Ï•6. Virology 272:218–224

    Article  PubMed  CAS  Google Scholar 

  • Hsiao J, Martinez-Costas J, Benavente J, Vakharia VN (2002) Cloning, expression, and characterization of avian reovirus guanylyltransferase. Virology 296:288–299

    Article  PubMed  CAS  Google Scholar 

  • Huiskonen JT, de Haas F, Bubeck D, Bamford DH, Fuller SD, Butcher SJ (2006) Structure of the bacteriophage Ï•6 nucleocapsid suggests a mechanism for sequential RNA packaging. Structure 14:1039–1048

    Article  PubMed  CAS  Google Scholar 

  • Huiskonen JT, Jaalinoja HT, Briggs JA, Fuller SD, Butcher SJ (2007) Structure of a hexameric RNA packaging motor in a viral polymerase complex. J Struct Biol 158:156–164

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki K, Miyazaki N, Hammar L, Zhu Y, Omura T, Wu B, Sjoborg F, Yonekura K, Murata K, Namba K, Caspar DL, Fujiyoshi Y, Cheng RH (2008) Pleomorphic configuration of the trimeric capsid proteins of Rice dwarf virus that allows formation of both the outer capsid and tubular crystals. J Mol Biol 383:252–265

    Article  PubMed  CAS  Google Scholar 

  • Jaalinoja HT, Huiskonen JT, Butcher SJ (2007) Electron cryomicroscopy comparison of the architectures of the enveloped bacteriophages Ï•6 and Ï•8. Structure 15:157–167

    Article  PubMed  CAS  Google Scholar 

  • Jane-Valbuena J, Nibert ML, Spencer SM, Walker SB, Baker TS, Chen Y, Centonze VE, Schiff LA (1999) Reovirus virion-like particles obtained by recoating infectious subvirion particles with baculovirus-expressed σ3 protein: an approach for analyzing σ3 functions during virus entry. J Virol 73:2963–2973

    PubMed  CAS  Google Scholar 

  • Jayaram H, Taraporewala Z, Patton JT, Prasad BV (2002) Rotavirus protein involved in genome replication and packaging exhibits a HIT-like fold. Nature 417:311–315

    Article  PubMed  CAS  Google Scholar 

  • Juuti JT, Bamford DH (1995) RNA binding, packaging and polymerase activities of the different incomplete polymerase complex particles of dsRNA bacteriophage Ï•6. J Mol Biol 249:545–554

    Article  PubMed  CAS  Google Scholar 

  • Juuti JT, Bamford DH (1997) Protein P7 of phage Ï•6 RNA polymerase complex, acquiring of RNA packaging activity by in vitro assembly of the purified protein onto deficient particles. J Mol Biol 266:891–900

    Article  PubMed  CAS  Google Scholar 

  • Juuti JT, Bamford DH, Tuma R, Thomas GJ Jr (1998) Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage Ï•6. J Mol Biol 279:347–359

    Article  PubMed  CAS  Google Scholar 

  • Kainov DE, Butcher SJ, Bamford DH, Tuma R (2003a) Conserved intermediates on the assembly pathway of double-stranded RNA bacteriophages. J Mol Biol 328:791–804

    Article  PubMed  CAS  Google Scholar 

  • Kainov DE, Pirttimaa M, Tuma R, Butcher SJ, Thomas GJ Jr, Bamford DH, Makeyev EV (2003b) RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J Biol Chem 278:48084–48091

    Article  PubMed  CAS  Google Scholar 

  • Kainov DE, Lisal J, Bamford DH, Tuma R (2004) Packaging motor from double-stranded RNA bacteriophage Ï•12 acts as an obligatory passive conduit during transcription. Nucleic Acids Res 32:3515–3521

    Article  PubMed  CAS  Google Scholar 

  • Kar AK, Roy P (2003) Defining the structure-function relationships of bluetongue virus helicase protein VP6. J Virol 77:11347–11356

    Article  PubMed  CAS  Google Scholar 

  • Kar AK, Ghosh M, Roy P (2004) Map** the assembly pathway of Bluetongue virus scaffolding protein VP3. Virology 324:387–399

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Zhang X, Centonze VE, Bowman VD, Noble S, Baker TS, Nibert ML (2002) The hydrophilic amino-terminal arm of reovirus core shell protein λ1 is dispensable for particle assembly. J Virol 76:12211–12222

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Parker JS, Murray KE, Nibert ML (2004) Nucleoside and RNA triphosphatase activities of orthoreovirus transcriptase cofactor μ2. J Biol Chem 279:4394–4403

    Article  PubMed  CAS  Google Scholar 

  • Labbe M, Charpilienne A, Crawford SE, Estes MK, Cohen J (1991) Expression of rotavirus VP2 produces empty corelike particles. J Virol 65:2946–2952

    PubMed  CAS  Google Scholar 

  • Laurinavicius S, Kakela R, Bamford DH, Somerharju P (2004) The origin of phospholipids of the enveloped bacteriophage phi6. Virology 326:182–190

    Article  PubMed  CAS  Google Scholar 

  • Lawton JA, Estes MK, Prasad BV (1997a) Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat Struct Biol 4:118–121

    Article  PubMed  CAS  Google Scholar 

  • Lawton JA, Zeng CQ, Mukherjee SK, Cohen J, Estes MK, Prasad BV (1997b) Three-dimensional structural analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer. J Virol 71:7353–7360

    PubMed  CAS  Google Scholar 

  • Le Blois H, French T, Mertens PP, Burroughs JN, Roy P (1992) The expressed VP4 protein of bluetongue virus binds GTP and is the candidate guanylyl transferase of the virus. Virology 189:757–761

    Article  PubMed  Google Scholar 

  • Lepault J, Petitpas I, Erk I, Navaza J, Bigot D, Dona M, Vachette P, Cohen J, Rey FA (2001) Structural polymorphism of the major capsid protein of rotavirus. EMBO J 20:1498–1507

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Baker ML, Jiang W, Estes MK, Prasad BV (2009) Rotavirus architecture at subnanometer resolution. J Virol 83:1754–1766

    Article  PubMed  CAS  Google Scholar 

  • Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC (2002) Structure of the reovirus membrane-penetration protein, μ1, in a complex with its protector protein, σ3. Cell 108:283–295

    Article  PubMed  CAS  Google Scholar 

  • Liu M, Mattion NM, Estes MK (1992) Rotavirus VP3 expressed in insect cells possesses guanylyltransferase activity. Virology 188:77–84

    Article  PubMed  CAS  Google Scholar 

  • Loudon PT, Roy P (1992) Interaction of nucleic acids with core-like and subcore-like particles of bluetongue virus. Virology 191:231–236

    Article  PubMed  CAS  Google Scholar 

  • Lu G, Zhou ZH, Baker ML, Jakana J, Cai D, Wei X, Chen S, Gu X, Chiu W (1998) Structure of double-shelled rice dwarf virus. J Virol 72:8541–8549

    PubMed  CAS  Google Scholar 

  • Lu X, McDonald SM, Tortorici MA, Tao YJ, Vasquez-Del Carpio R, Nibert ML, Patton JT, Harrison SC (2008) Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure 16:1678–1688

    Article  PubMed  CAS  Google Scholar 

  • Luongo CL, Zhang X, Walker SB, Chen Y, Broering TJ, Farsetta DL, Bowman VD, Baker TS, Nibert ML (2002) Loss of activities for mRNA synthesis accompanies loss of λ2 spikes from reovirus cores: an effect of λ2 on λ1 shell structure. Virology 296:24–38

    Article  PubMed  CAS  Google Scholar 

  • Luque D, Gonzalez JM, Garriga D, Ghabrial SA, Havens WM, Trus B, Verdaguer N, Carrascosa JL, Caston JR (2010) The T  =  1 capsid protein of Penicillium chrysogenum virus is formed by a repeated helix-rich core indicative of gene duplication. J Virol 84:7256–7266

    Article  PubMed  CAS  Google Scholar 

  • Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, Pothier P, Prasad BV, Cohen J, Rey FA (2001) Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. EMBO J 20:1485–1497

    Article  PubMed  CAS  Google Scholar 

  • Matsuo E, Roy P (2009) Bluetongue virus VP6 acts early in the replication cycle and can form the basis of chimeric virus formation. J Virol 83:8842–8848

    Article  PubMed  CAS  Google Scholar 

  • McClain B, Settembre E, Temple BR, Bellamy AR, Harrison SC (2010) X-ray crystal structure of the rotavirus inner capsid particle at 3.8 Ã… resolution. J Mol Biol 397:587–599

    Article  PubMed  CAS  Google Scholar 

  • Mendez II, Weiner SG, She YM, Yeager M, Coombs KM (2008) Conformational changes accompany activation of reovirus RNA-dependent RNA transcription. J Struct Biol 162:277–289

    Article  PubMed  CAS  Google Scholar 

  • Mertens P (2004) The dsRNA viruses. Virus Res 101:3–13

    Article  PubMed  CAS  Google Scholar 

  • Miller CL, Arnold MM, Broering TJ, Hastings CE, Nibert ML (2010) Localization of mammalian orthoreovirus proteins to cytoplasmic factory-like structures via nonoverlap** regions of μ NS. J Virol 84:867–882

    Article  PubMed  CAS  Google Scholar 

  • Mindich L, Lehman J (1979) Cell wall lysin as a component of the bacteriophage Ï•6 virion. J Virol 30:489–496

    PubMed  CAS  Google Scholar 

  • Mindich L, Qiao X, Onodera S, Gottlieb P, Frilander M (1994) RNA structural requirements for stability and minus-strand synthesis in the dsRNA bacteriophage Ï•6. Virology 202:258–263

    Article  PubMed  CAS  Google Scholar 

  • Mindich L, Qiao X, Qiao J, Onodera S, Romantschuk M, Hoogstraten D (1999) Isolation of additional bacteriophages with genomes of segmented double-stranded RNA. J Bacteriol 181:4505–4508

    PubMed  CAS  Google Scholar 

  • Miyazaki N, Wu B, Hagiwara K, Wang CY, **ng L, Hammar L, Higashiura A, Tsukihara T, Nakagawa A, Omura T, Cheng RH (2010) The functional organization of the internal components of Rice dwarf virus. J Biochem 147:843–850

    Article  PubMed  CAS  Google Scholar 

  • Moss SR, Nuttall PA (1994) Subcore- and core-like particles of Broadhaven virus (BRDV), a tick-borne orbivirus, synthesized from baculovirus expressed VP2 and VP7, the major core proteins of BRDV. Virus Res 32:401–407

    Article  PubMed  CAS  Google Scholar 

  • Naitow H, Tang J, Canady M, Wickner RB, Johnson JE (2002) L-A virus at 3.4 Ã… resolution reveals particle architecture and mRNA decap** mechanism. Nat Struct Biol 9:725–728

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa A, Miyazaki N, Taka J, Naitow H, Ogawa A, Fujimoto Z, Mizuno H, Higashi T, Watanabe Y, Omura T, Cheng RH, Tsukihara T (2003) The atomic structure of rice dwarf virus reveals the self-assembly mechanism of component proteins. Structure 11:1227–1238

    Article  PubMed  CAS  Google Scholar 

  • Nason EL, Samal SK, Venkataram Prasad BV (2000) Trypsin-induced structural transformation in aquareovirus. J Virol 74:6546–6555

    Article  PubMed  CAS  Google Scholar 

  • Nason EL, Rothagel R, Mukherjee SK, Kar AK, Forzan M, Prasad BV, Roy P (2004) Interactions between the inner and outer capsids of bluetongue virus. J Virol 78:8059–8067

    Article  PubMed  CAS  Google Scholar 

  • Nibert ML, Fields BN (1992) A carboxy-terminal fragment of protein μ1/μ1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66:6408–6418

    PubMed  CAS  Google Scholar 

  • Nibert ML, Odegard AL, Agosto MA, Chandran K, Schiff LA (2005) Putative autocleavage of reovirus μ1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J Mol Biol 345:461–474

    Article  PubMed  CAS  Google Scholar 

  • Olkkonen VM, Gottlieb P, Strassman J, Qiao XY, Bamford DH, Mindich L (1990) In vitro assembly of infectious nucleocapsids of bacteriophage Ï•6: formation of a recombinant double-stranded RNA virus. Proc Natl Acad Sci USA 87:9173–9177

    Article  PubMed  CAS  Google Scholar 

  • Olkkonen VM, Ojala PM, Bamford DH (1991) Generation of infectious nucleocapsids by in vitro assembly of the shell protein on to the polymerase complex of the dsRNA bacteriophage Ï•6. J Mol Biol 218:569–581

    Article  PubMed  CAS  Google Scholar 

  • Paatero AO, Mindich L, Bamford DH (1998) Mutational analysis of the role of nucleoside triphosphatase P4 in the assembly of the RNA polymerase complex of bacteriophage Ï•6. J Virol 72:10058–10065

    PubMed  CAS  Google Scholar 

  • Pan J, Vakharia VN, Tao YJ (2007) The structure of a birnavirus polymerase reveals a distinct active site topology. Proc Natl Acad Sci USA 104:7385–7390

    Article  PubMed  CAS  Google Scholar 

  • Pan J, Dong L, Lin L, Ochoa WF, Sinkovits RS, Havens WM, Nibert ML, Baker TS, Ghabrial SA, Tao YJ (2009) Atomic structure reveals the unique capsid organization of a dsRNA virus. Proc Natl Acad Sci USA 106:4225–4230

    Article  PubMed  CAS  Google Scholar 

  • Patton JT, Gallegos CO (1990) Rotavirus RNA replication: single-stranded RNA extends from the replicase particle. J Gen Virol 71:1087–1094

    Article  PubMed  CAS  Google Scholar 

  • Patton JT, Spencer E (2000) Genome replication and packaging of segmented double-stranded RNA viruses. Virology 277:217–225

    Article  PubMed  CAS  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  PubMed  CAS  Google Scholar 

  • Pirttimaa MJ, Bamford DH (2000) RNA secondary structures of the bacteriophage Ï•6 packaging regions. RNA 6:880–889

    Article  PubMed  CAS  Google Scholar 

  • Pirttimaa MJ, Paatero AO, Frilander MJ, Bamford DH (2002) Nonspecific nucleoside triphosphatase P4 of double-stranded RNA bacteriophage Ï•6 is required for single-stranded RNA packaging and transcription. J Virol 76:10122–10127

    Article  PubMed  CAS  Google Scholar 

  • Poranen MM, Bamford DH (1999) Packaging and replication regulation revealed by chimeric genome segments of double-stranded RNA bacteriophage Ï•6. RNA 5:446–454

    Article  PubMed  CAS  Google Scholar 

  • Poranen MM, Bamford DH (2011) Cystovirus, cystoviridae. In: Tidona C, Darai G (eds) Springer index of viruses, 2nd edn. Springer, New York

    Google Scholar 

  • Poranen MM, Daugelavicius R, Ojala PM, Hess MW, Bamford DH (1999) A novel virus-host cell membrane interaction. Membrane voltage-dependent endocytic-like entry of bacteriophage straight Ï•6 nucleocapsid. J Cell Biol 147:671–682

    Article  PubMed  CAS  Google Scholar 

  • Poranen MM, Paatero AO, Tuma R, Bamford DH (2001) Self-assembly of a viral molecular machine from purified protein and RNA constituents. Mol Cell 7:845–854

    Article  PubMed  CAS  Google Scholar 

  • Poranen MM, Pirttimaa MJ, Bamford DH (2005a) Encapsidation of the segmented double-stranded RNA genome of bacteriophage Ï•6. In: Catalano C (ed) Viral genome packaging machines: genetics, structure, and mechanism. Kluwer, New York, pp 117–134

    Chapter  Google Scholar 

  • Poranen MM, Tuma R, Bamford DH (2005b) Assembly of double-stranded RNA bacteriophages. Adv Virus Res 64:15–43

    Article  PubMed  CAS  Google Scholar 

  • Poranen MM, Butcher SJ, Simonov VM, Laurinmaki P, Bamford DH (2008) Roles of the minor capsid protein P7 in the assembly and replication of double-stranded RNA bacteriophage Ï•6. J Mol Biol 383:529–538

    Article  PubMed  CAS  Google Scholar 

  • Prasad BV, Wang GJ, Clerx JP, Chiu W (1988) Three-dimensional structure of rotavirus. J Mol Biol 199:269–275

    Article  PubMed  CAS  Google Scholar 

  • Prasad BV, Burns JW, Marietta E, Estes MK, Chiu W (1990) Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy. Nature 343:476–479

    Article  PubMed  CAS  Google Scholar 

  • Prasad BV, Rothnagel R, Zeng CQ, Jakana J, Lawton JA, Chiu W, Estes MK (1996) Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382:471–473

    Article  PubMed  CAS  Google Scholar 

  • Qiao X, Casini G, Qiao J, Mindich L (1995) In vitro packaging of individual genomic segments of bacteriophage Ï•6 RNA: serial dependence relationships. J Virol 69:2926–2931

    PubMed  CAS  Google Scholar 

  • Qiao X, Qiao J, Mindich L (2003) Analysis of specific binding involved in genomic packaging of the double-stranded-RNA bacteriophage Ï•6. J Bacteriol 185:6409–6414

    Article  PubMed  CAS  Google Scholar 

  • Qiao X, Sun Y, Qiao J, Di Sanzo F, Mindich L (2010) Characterization of Ï•2954, a newly isolated bacteriophage containing three dsRNA genomic segments. BMC Microbiol 10:55

    Article  PubMed  CAS  Google Scholar 

  • Ramadevi N, Burroughs NJ, Mertens PP, Jones IM, Roy P (1998a) Cap** and methylation of mRNA by purified recombinant VP4 protein of bluetongue virus. Proc Natl Acad Sci USA 95:13537–13542

    Article  PubMed  CAS  Google Scholar 

  • Ramadevi N, Rodriguez J, Roy P (1998b) A leucine zipper-like domain is essential for dimerization and encapsidation of bluetongue virus nucleocapsid protein VP4. J Virol 72:2983–2990

    PubMed  CAS  Google Scholar 

  • Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681

    Article  PubMed  CAS  Google Scholar 

  • Reddy VS, Johnson JE (2005) Structure-derived insights into virus assembly. Adv Virus Res 64:45–68

    Article  PubMed  CAS  Google Scholar 

  • Reinisch KM, Nibert ML, Harrison SC (2000) Structure of the reovirus core at 3.6 Ã… resolution. Nature 404:960–967

    Article  PubMed  CAS  Google Scholar 

  • Rohrmann GF (1986) Polyhedrin structure. J Gen Virol 67:1499–1513

    Article  PubMed  CAS  Google Scholar 

  • Rossmann MG, Johnson JE (1989) Icosahedral RNA virus structure. Annu Rev Biochem 58:533–573

    Article  PubMed  CAS  Google Scholar 

  • Roy P (2005) Bluetongue virus proteins and particles and their role in virus entry, assembly, and release. Adv Virus Res 64:69–123

    Article  PubMed  CAS  Google Scholar 

  • Schuck P, Taraporewala Z, McPhie P, Patton JT (2001) Rotavirus nonstructural protein NSP2 self-assembles into octamers that undergo ligand-induced conformational changes. J Biol Chem 276:9679–9687

    Article  PubMed  CAS  Google Scholar 

  • Sen A, Heymann JB, Cheng N, Qiao J, Mindich L, Steven AC (2008) Initial location of the RNA-dependent RNA polymerase in the bacteriophage Ï•6 procapsid determined by cryo-electron microscopy. J Biol Chem 283:12227–12231

    Article  PubMed  CAS  Google Scholar 

  • Settembre EC, Chen JZ, Dormitzer PR, Grigorieff N, Harrison SC (2011) Atomic model of an infectious rotavirus particle. EMBO J 30:408–416

    Article  PubMed  CAS  Google Scholar 

  • Shaw AL, Samal SK, Subramanian K, Prasad BV (1996) The structure of aquareovirus shows how the different geometries of the two layers of the capsid are reconciled to provide symmetrical interactions and stabilization. Structure 4:957–967

    Article  PubMed  CAS  Google Scholar 

  • Shimizu T, Yoshii M, Wei T, Hirochika H, Omura T (2009) Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of Rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol J 7:24–32

    Article  PubMed  CAS  Google Scholar 

  • Shing M, Coombs KM (1996) Assembly of the reovirus outer capsid requires μ1/σ3 interactions which are prevented by misfolded σ3 protein in temperature-sensitive mutant tsG453. Virus Res 46:19–29

    Article  PubMed  CAS  Google Scholar 

  • Spies U, Muller H, Becht H (1987) Properties of RNA polymerase activity associated with infectious bursal disease virus and characterization of its reaction products. Virus Res 8:127–140

    Article  PubMed  CAS  Google Scholar 

  • Stauber N, Martinez-Costas J, Sutton G, Monastyrskaya K, Roy P (1997) Bluetongue virus VP6 protein binds ATP and exhibits an RNA-dependent ATPase function and a helicase activity that catalyze the unwinding of double-stranded RNA substrates. J Virol 71:7220–7226

    PubMed  CAS  Google Scholar 

  • Sun Y, Qiao X, Qiao J, Onodera S, Mindich L (2003) Unique properties of the inner core of bacteriophage Ï•8, a virus with a segmented dsRNA genome. Virology 308:354–361

    Article  PubMed  CAS  Google Scholar 

  • Tan BH, Nason E, Staeuber N, Jiang W, Monastryrskaya K, Roy P (2001) RGD tripeptide of bluetongue virus VP7 protein is responsible for core attachment to Culicoides cells. J Virol 75:3937–3947

    Article  PubMed  CAS  Google Scholar 

  • Tan YR, Sun JC, Lu XY, Su DM, Zhang JQ (2003) Entry of Bombyx mori cypovirus 1 into midgut cells in vivo. J Electron Microsc (Tokyo) 52:485–489

    Article  Google Scholar 

  • Tao Y, Farsetta DL, Nibert ML, Harrison SC (2002) RNA synthesis in a cage – structural studies of reovirus polymerase λ3. Cell 111:733–745

    Article  PubMed  CAS  Google Scholar 

  • Taraporewala ZF, Patton JT (2001) Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J Virol 75:4519–4527

    Article  PubMed  CAS  Google Scholar 

  • Taraporewala ZF, Patton JT (2004) Nonstructural proteins involved in genome packaging and replication of rotaviruses and other members of the Reoviridae. Virus Res 101:57–66

    Article  PubMed  CAS  Google Scholar 

  • Taraporewala Z, Chen D, Patton JT (1999) Multimers formed by the rotavirus nonstructural protein NSP2 bind to RNA and have nucleoside triphosphatase activity. J Virol 73:9934–9943

    PubMed  CAS  Google Scholar 

  • Taraporewala ZF, Jiang X, Vasquez-Del Carpio R, Jayaram H, Prasad BV, Patton JT (2006) Structure-function analysis of rotavirus NSP2 octamer by using a novel complementation system. J Virol 80:7984–7994

    Article  PubMed  CAS  Google Scholar 

  • Thomas CP, Booth TF, Roy P (1990) Synthesis of bluetongue virus-encoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J Gen Virol 71:2073–2083

    Article  PubMed  CAS  Google Scholar 

  • Tortorici MA, Broering TJ, Nibert ML, Patton JT (2003) Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus. J Biol Chem 278:32673–32682

    Article  PubMed  CAS  Google Scholar 

  • Tortorici MA, Shapiro BA, Patton JT (2006) A base-specific recognition signal in the 5′ consensus sequence of rotavirus plus-strand RNAs promotes replication of the double-stranded RNA genome segments. RNA 12:133–146

    Article  PubMed  CAS  Google Scholar 

  • Ueda S, Masuta C, Uyeda I (1997) Hypothesis on particle structure and assembly of rice dwarf phytoreovirus: interactions among multiple structural proteins. J Gen Virol 78:3135–3140

    PubMed  CAS  Google Scholar 

  • Usala SJ, Brownstein BH, Haselkorn R (1980) Displacement of parental RNA strands during in vitro transcription by bacteriophage Ï•6 nucleocapsids. Cell 19:855–862

    Article  PubMed  CAS  Google Scholar 

  • Wei T, Shimizu T, Hagiwara K, Kikuchi A, Moriyasu Y, Suzuki N, Chen H, Omura T (2006) Pns12 protein of Rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J Gen Virol 87:429–438

    Article  PubMed  CAS  Google Scholar 

  • Wei H, Cheng RH, Berriman J, Rice WJ, Stokes DL, Katz A, Morgan DG, Gottlieb P (2009) Three-dimensional structure of the enveloped bacteriophage Ï•12: an incomplete T  =  13 lattice is superposed on an enclosed T  =  1 shell. PLoS One 4:e6850

    Article  PubMed  CAS  Google Scholar 

  • Wu B, Hammar L, **ng L, Markarian S, Yan J, Iwasaki K, Fujiyoshi Y, Omura T, Cheng RH (2000) Phytoreovirus T  =  1 core plays critical roles in organizing the outer capsid of T  =  13 quasi-equivalence. Virology 271:18–25

    Article  PubMed  CAS  Google Scholar 

  • Xu P, Miller SE, Joklik WK (1993) Generation of reovirus core-like particles in cells infected with hybrid vaccinia viruses that express genome segments L1, L2, L3, and S2. Virology 197:726–731

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Wilson W, Mecham J, Murphy K, Zhou EM, Tabachnick W (1997) VP7: an attachment protein of bluetongue virus for cellular receptors in Culicoides variipennis. J Gen Virol 78:1617–1623

    PubMed  CAS  Google Scholar 

  • Yan J, Tomaru M, Takahashi A, Kimura I, Hibino H, Omura T (1996) P2 protein encoded by genome segment S2 of rice dwarf phytoreovirus is essential for virus infection. Virology 224:539–541

    Article  PubMed  CAS  Google Scholar 

  • Yu X, ** L, Zhou ZH (2008) 3.88 Ã… structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 453:415–419

    Article  PubMed  CAS  Google Scholar 

  • Zeng CQ, Wentz MJ, Cohen J, Estes MK, Ramig RF (1996) Characterization and replicase activity of double-layered and single-layered rotavirus-like particles expressed from baculovirus recombinants. J Virol 70:2736–2742

    PubMed  CAS  Google Scholar 

  • Zhang X, Walker SB, Chipman PR, Nibert ML, Baker TS (2003) Reovirus polymerase λ3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Ã…. Nat Struct Biol 10:1011–1018

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, ** L, Fang Q, Hui WH, Zhou ZH (2010) 3.3 Ã… cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 141:472–482

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Boyce M, Bhattacharya B, Schein S, Roy P, Zhou ZH (2011) Bluetongue virus coat protein VP2 contains sialic acid-binding domains, and VP5 resembles enveloped virus fusion proteins. Proc Natl Acad Sci USA 107:6292–6297

    Article  Google Scholar 

  • Zheng H, Yu L, Wei C, Hu D, Shen Y, Chen Z, Li Y (2000) Assembly of double-shelled, virus-like particles in transgenic rice plants expressing two major structural proteins of rice dwarf virus. J Virol 74:9808–9810

    Article  PubMed  CAS  Google Scholar 

  • Zhong B, Kikuchi A, Moriyasu Y, Higashi T, Hagiwara K, Omura T (2003) A minor outer capsid protein, P9, of Rice dwarf virus. Arch Virol 148:2275–2280

    Article  PubMed  CAS  Google Scholar 

  • Zhou F, Pu Y, Wei T, Liu H, Deng W, Wei C, Ding B, Omura T, Li Y (2007) The P2 capsid protein of the nonenveloped rice dwarf phytoreovirus induces membrane fusion in insect host cells. Proc Natl Acad Sci USA 104:19547–19552

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Hemmings AM, Iwasaki K, Fujiyoshi Y, Zhong B, Yan J, Isogai M, Omura T (1997) Details of the arrangement of the outer capsid of rice dwarf phytoreovirus, as visualized by two-dimensional crystallography. J Virol 71:8899–8901

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Finnish Center of Excellence Program (2006–2011) of the Academy of Finland (grant 1129684) and Academy of Finland grants 250113 and 256069.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Minna M. Poranen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Poranen, M.M., Bamford, D.H. (2012). Assembly of Large Icosahedral Double-Stranded RNA Viruses. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9_17

Download citation

Publish with us

Policies and ethics

Navigation